The fate of organic carbon reserves sequestered in permafrost is uncertain yet critically important for addressing terrestrial feedbacks to climate change. With warming there is an increased probability of thermokarst formation, and an increase in CO2 and CH4 flux to the atmosphere. However, we understand little of the underlying microbial controls on nitrogen or carbon cycling in permafrost soils. We applied a variety of omics methods to study microbial communities, their functions and activity in permafrost soils collected from two sites in Alaska: a stable, low productivity black spruce forest, and a thermokarst bog at the Bonanza Creek LTER Station outside of Fairbanks.
Each zone (active layer, permafrost, and bog) had a unique complement of genes, transcripts and proteins, indicative of differences in microbial community composition and their functional potentials. The most abundant bacteria in permafrost soil, based on 16S rRNA gene sequences, were members of phyla Chloroflexi, Proteobacteria and Actinobacteria. Similar phylogenetic distributions were observed in metagenome and metatranscriptome datasets. Of the functions iron reduction emerged as a potential metabolic strategy employed by microbes in permafrost. By contrast, the active layer communities expressed genes and proteins involved in obtaining energy and nutrients from a diversity of aerobic and anaerobic processes and were equipped with functions for survival under freeze-thaw conditions. The thermokarst bog was dominated by anaerobic methanogens that support high rates of methanogenesis.
We binned the metagenomic contigs based on tetranucelotide frequency, and taxonomic assignment of the largest bins were to uncultured Deltaproteobacteria and Actinobacteria. Likewise, the single cell sequencing from permafrost resulted in a Chloroflexi and Deltaproteobacteria genomes. The Chloroflexi SAG had genes for iron and nitrate reduction, and mechanisms to tolerate oxidative and redox stress. The Deltaproteobacteria SAG contained for nitrogen fixation, carbohydrate and sulfate transporters and osmoprotectants as well as pathways to tolerate various stressors in freezing soil.
These analyses reveal energy-yielding microbial processes and potential strategies for microbial survival in permafrost soils, and linkages between biogeochemical process rates and omics measurements. The results provide new knowledge about microbial life and potential activities in permafrost, particularly iron reduction, and display linkages between microbial gene expression and rates of microbial processes, especially in methanogenesis following thaw. The multi-omics strategy demonstrated here enables better mechanistic understanding of the ecological strategies utilized by soil microbial communities in response to future climate change.